{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,17]],"date-time":"2026-09-17T19:36:06Z","timestamp":1789673766892,"version":"4.0.1"},"reference-count":119,"publisher":"Cambridge University Press (CUP)","license":[{"start":{"date-parts":[[2022,9,21]],"date-time":"2022-09-21T00:00:00Z","timestamp":1663718400000},"content-version":"unspecified","delay-in-days":263,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["cambridge.org"],"crossmark-restriction":true},"short-container-title":["Epidemiol. Infect."],"published-print":{"date-parts":[[2022]]},"abstract":"<jats:title>Abstract<\/jats:title>\n\t  <jats:p>Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) caused the novel global coronavirus disease 2019 (COVID-19) disease outbreak. Its pathogenesis is mostly located in the respiratory tract. However, other organs are also affected. Hence, realising how such a complex disturbance affects patients after recovery is crucial. Regarding the significance of control of COVID-19-related complications after recovery, the current study was designed to review the cellular and molecular mechanisms linking COVID-19 to significant long-term signs including renal and cardiac complications, cutaneous and neurological manifestations, as well as blood coagulation disorders. This virus can directly influence on the cells through Angiotensin converting enzyme 2 (ACE-2) to induce cytokine storm. Acute release of Interleukin-1 (IL1), IL6 and plasminogen activator inhibitor 1 (PAI-1) have been related to elevating risk of heart failure. Also, inflammatory cytokines like IL-8 and Tumour necrosis factor-<jats:italic>\u03b1<\/jats:italic> cause the secretion of von Willebrand factor (VWF) from human endothelial cells and then VWF binds to Neutrophil extracellular traps to induce thrombosis. On the other hand, the virus can damage the blood\u2013brain barrier by increasing its permeability and subsequently enters into the central nervous system and the systemic circulation. Furthermore, SARS-induced ACE2-deficiency decreases [des-Arg9]-bradykinin (desArg9-BK) degradation in kidneys to induce inflammation, thrombotic problems, fibrosis and necrosis. Notably, the angiotensin II-angiotensin II type 1 receptor binding causes an increase in aldosterone and mineralocorticoid receptors on the surface of dendritic cells cells, leading to recalling macrophage and monocyte into inflammatory sites of skin. In conclusions, all the pathways play a key role in the pathogenesis of these disturbances. Nevertheless, more investigations are necessary to determine more pathogenetic mechanisms of the virus.<\/jats:p>","DOI":"10.1017\/s0950268822001480","type":"journal-article","created":{"date-parts":[[2022,9,21]],"date-time":"2022-09-21T06:47:16Z","timestamp":1663742836000},"update-policy":"https:\/\/doi.org\/10.1017\/policypage","source":"Crossref","is-referenced-by-count":9,"title":["Renal, cardiac, neurological, cutaneous and coagulopathic long-term manifestations of COVID-19 after recovery; A review"],"prefix":"10.1017","volume":"150","author":[{"given":"Reza","family":"Afrisham","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yasaman","family":"Jadidi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maryam","family":"Davoudi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kiana","family":"Moayedi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Saina","family":"Karami","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sahar","family":"Sadegh-Nejadi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Damoon","family":"Ashtary-Larky","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"ShadiSadat","family":"Seyyedebrahimi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1716-7072","authenticated-orcid":false,"given":"Shaban","family":"Alizadeh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"56","published-online":{"date-parts":[[2022,9,21]]},"reference":[{"key":"S0950268822001480_ref92","doi-asserted-by":"publisher","DOI":"10.1016\/j.thromres.2020.04.013"},{"key":"S0950268822001480_ref84","doi-asserted-by":"publisher","DOI":"10.4049\/jimmunol.0802886"},{"key":"S0950268822001480_ref96","doi-asserted-by":"publisher","DOI":"10.1159\/000453002"},{"key":"S0950268822001480_ref85","doi-asserted-by":"publisher","DOI":"10.1016\/j.clindermatol.2021.07.001"},{"key":"S0950268822001480_ref4","doi-asserted-by":"publisher","DOI":"10.1016\/j.biopha.2020.111200"},{"key":"S0950268822001480_ref25","doi-asserted-by":"publisher","DOI":"10.1097\/01.ASN.0000127988.42710.A7"},{"key":"S0950268822001480_ref59","doi-asserted-by":"publisher","DOI":"10.3389\/fnagi.2021.653694"},{"key":"S0950268822001480_ref64","doi-asserted-by":"publisher","DOI":"10.3389\/fnmol.2020.556175"},{"key":"S0950268822001480_ref89","doi-asserted-by":"publisher","DOI":"10.1126\/scitranslmed.abd3876"},{"key":"S0950268822001480_ref14","doi-asserted-by":"publisher","DOI":"10.1016\/j.peptides.2020.170428"},{"key":"S0950268822001480_ref17","doi-asserted-by":"publisher","DOI":"10.1159\/000520235"},{"key":"S0950268822001480_ref108","doi-asserted-by":"publisher","DOI":"10.1007\/s00134-020-06062-x"},{"key":"S0950268822001480_ref70","doi-asserted-by":"publisher","DOI":"10.1590\/0004-282x20200089"},{"key":"S0950268822001480_ref29","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-021-22781-1"},{"key":"S0950268822001480_ref119","doi-asserted-by":"publisher","DOI":"10.1097\/HS9.0000000000000526"},{"key":"S0950268822001480_ref30","doi-asserted-by":"publisher","DOI":"10.1093\/ndt\/gfab042"},{"key":"S0950268822001480_ref68","first-page":"4221","article-title":"Neuropilin-1 as a new potential SARS-CoV-2 infection mediator implicated in the neurologic features and central nervous system involvement of COVID-19","volume":"22","author":"Davies","year":"2020","journal-title":"Molecular Medicine Reports"},{"key":"S0950268822001480_ref57","doi-asserted-by":"publisher","DOI":"10.1016\/j.ijid.2021.01.002"},{"key":"S0950268822001480_ref114","doi-asserted-by":"publisher","DOI":"10.1007\/s11739-020-02394-0"},{"key":"S0950268822001480_ref101","doi-asserted-by":"publisher","DOI":"10.1161\/ATVBAHA.120.315267"},{"key":"S0950268822001480_ref18","doi-asserted-by":"publisher","DOI":"10.1681\/ASN.2006050423"},{"key":"S0950268822001480_ref39","doi-asserted-by":"publisher","DOI":"10.1038\/s41569-020-0360-5"},{"key":"S0950268822001480_ref95","doi-asserted-by":"publisher","DOI":"10.1038\/nri3345"},{"key":"S0950268822001480_ref2","first-page":"8750","article-title":"Gastrointestinal manifestations in COVID-19 infection and its practical applications","volume":"12","author":"Mandal","year":"2020","journal-title":"Cureus"},{"key":"S0950268822001480_ref51","first-page":"1","article-title":"Neurological sequelae of COVID-19: a review. The Egyptian Journal of Neurology","volume":"57","author":"Peterson","year":"2021","journal-title":"Psychiatry and Neurosurgery"},{"key":"S0950268822001480_ref20","doi-asserted-by":"publisher","DOI":"10.1161\/01.RES.87.5.e1"},{"key":"S0950268822001480_ref77","doi-asserted-by":"publisher","DOI":"10.1111\/bjd.19327"},{"key":"S0950268822001480_ref16","doi-asserted-by":"publisher","DOI":"10.1007\/s11906-017-0778-2"},{"key":"S0950268822001480_ref116","doi-asserted-by":"publisher","DOI":"10.1111\/jth.14844"},{"key":"S0950268822001480_ref7","doi-asserted-by":"publisher","DOI":"10.1093\/cid\/ciaa149"},{"key":"S0950268822001480_ref12","doi-asserted-by":"publisher","DOI":"10.1017\/S095026882200125X"},{"key":"S0950268822001480_ref42","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2249.2004.02415.x"},{"key":"S0950268822001480_ref105","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-med-061813-013241"},{"key":"S0950268822001480_ref52","doi-asserted-by":"publisher","DOI":"10.1002\/jcla.24403"},{"key":"S0950268822001480_ref65","doi-asserted-by":"publisher","DOI":"10.1111\/ane.13266"},{"key":"S0950268822001480_ref45","doi-asserted-by":"publisher","DOI":"10.1016\/j.hrthm.2020.06.016"},{"key":"S0950268822001480_ref38","doi-asserted-by":"publisher","DOI":"10.1080\/14787210.2020.1822737"},{"key":"S0950268822001480_ref75","doi-asserted-by":"publisher","DOI":"10.1111\/all.14498"},{"key":"S0950268822001480_ref36","doi-asserted-by":"publisher","DOI":"10.1161\/JAHA.120.016219"},{"key":"S0950268822001480_ref87","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2011.07.033"},{"key":"S0950268822001480_ref40","doi-asserted-by":"publisher","DOI":"10.1016\/S0140-6736(20)30183-5"},{"key":"S0950268822001480_ref110","doi-asserted-by":"publisher","DOI":"10.1016\/j.thromres.2020.05.017"},{"key":"S0950268822001480_ref19","doi-asserted-by":"publisher","DOI":"10.1016\/0162-3109(95)00011-H"},{"key":"S0950268822001480_ref90","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2020.09.016"},{"key":"S0950268822001480_ref66","doi-asserted-by":"publisher","DOI":"10.1016\/j.isci.2020.101839"},{"key":"S0950268822001480_ref72","doi-asserted-by":"publisher","DOI":"10.1186\/s10194-020-01165-8"},{"key":"S0950268822001480_ref21","first-page":"2188","article-title":"Clinical profile, outcome and management of kidney disease in COVID-19 patients\u2013a narrative review","volume":"26","author":"Vahdat","year":"2022","journal-title":"European Review for Medical and Pharmacological Sciences"},{"key":"S0950268822001480_ref104","doi-asserted-by":"publisher","DOI":"10.1007\/s00018-014-1743-8"},{"key":"S0950268822001480_ref99","doi-asserted-by":"publisher","DOI":"10.1111\/bjh.14077"},{"key":"S0950268822001480_ref34","doi-asserted-by":"publisher","DOI":"10.1016\/j.hrthm.2020.06.026"},{"key":"S0950268822001480_ref55","doi-asserted-by":"publisher","DOI":"10.1007\/s00405-020-05965-1"},{"key":"S0950268822001480_ref74","doi-asserted-by":"publisher","DOI":"10.1002\/jmv.27391"},{"key":"S0950268822001480_ref41","first-page":"E006","article-title":"Myocardial injury in patients with COVID-19 pneumonia","volume":"48","author":"Wei","year":"2020","journal-title":"Zhonghua xin xue guan bing za zhi"},{"key":"S0950268822001480_ref13","first-page":"1","article-title":"Mechanisms of COVID-19-induced kidney injury and current pharmacotherapies","volume":"71","author":"Faour","year":"2021","journal-title":"Inflammation Research"},{"key":"S0950268822001480_ref91","first-page":"763","article-title":"COVID-19 and venous thromboembolism: a meta-analysis of literature studies. in seminars in thrombosis and hemostasis","volume":"46","author":"Di Minno","year":"2020","journal-title":"Thieme Medical Publishers"},{"key":"S0950268822001480_ref63","doi-asserted-by":"publisher","DOI":"10.3390\/v12010014"},{"key":"S0950268822001480_ref8","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-021-95565-8"},{"key":"S0950268822001480_ref76","doi-asserted-by":"publisher","DOI":"10.2147\/CCID.S325552"},{"key":"S0950268822001480_ref9","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2020.02.052"},{"key":"S0950268822001480_ref82","doi-asserted-by":"publisher","DOI":"10.1017\/S0950268821001333"},{"key":"S0950268822001480_ref86","doi-asserted-by":"crossref","first-page":"1720","DOI":"10.1055\/s-0040-1715835","article-title":"Mannose-binding lectin is associated with thrombosis and coagulopathy in critically ill COVID-19 patients","volume":"120","author":"Eriksson","year":"2020","journal-title":"Thrombosis and Haemostasis"},{"key":"S0950268822001480_ref118","doi-asserted-by":"publisher","DOI":"10.1111\/jth.14871"},{"key":"S0950268822001480_ref83","doi-asserted-by":"publisher","DOI":"10.1016\/j.det.2021.05.008"},{"key":"S0950268822001480_ref31","doi-asserted-by":"publisher","DOI":"10.1161\/CIRCULATIONAHA.118.038529"},{"key":"S0950268822001480_ref43","doi-asserted-by":"publisher","DOI":"10.1007\/s12325-020-01399-7"},{"key":"S0950268822001480_ref106","doi-asserted-by":"publisher","DOI":"10.1097\/MBC.0000000000000065"},{"key":"S0950268822001480_ref53","doi-asserted-by":"publisher","DOI":"10.1007\/s00415-020-10067-3"},{"key":"S0950268822001480_ref22","doi-asserted-by":"publisher","DOI":"10.1016\/j.nefro.2021.09.002"},{"key":"S0950268822001480_ref62","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2020.621735"},{"key":"S0950268822001480_ref73","doi-asserted-by":"publisher","DOI":"10.3390\/ijms22041687"},{"key":"S0950268822001480_ref102","doi-asserted-by":"publisher","DOI":"10.1016\/S2666-5247(20)30144-0"},{"key":"S0950268822001480_ref49","doi-asserted-by":"publisher","DOI":"10.1016\/j.cbi.2018.07.008"},{"key":"S0950268822001480_ref71","first-page":"1","article-title":"Frequency of neurological presentations of coronavirus disease in patients presenting to a tertiary care hospital during the 2019 coronavirus disease pandemic","volume":"12","author":"Iltaf","year":"2020","journal-title":"Cureus"},{"key":"S0950268822001480_ref113","doi-asserted-by":"crossref","first-page":"1668","DOI":"10.1055\/s-0040-1715841","article-title":"Coagulopathy and thrombosis as a result of severe COVID-19 infection: a microvascular focus","volume":"120","author":"Katneni","year":"2020","journal-title":"Thrombosis and Haemostasis"},{"key":"S0950268822001480_ref27","doi-asserted-by":"publisher","DOI":"10.1038\/s41581-021-00452-0"},{"key":"S0950268822001480_ref80","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a011247"},{"key":"S0950268822001480_ref111","doi-asserted-by":"publisher","DOI":"10.1056\/NEJMc2013656"},{"key":"S0950268822001480_ref46","doi-asserted-by":"publisher","DOI":"10.1111\/jce.14479"},{"key":"S0950268822001480_ref61","doi-asserted-by":"publisher","DOI":"10.1016\/j.amsu.2022.104281"},{"key":"S0950268822001480_ref94","doi-asserted-by":"publisher","DOI":"10.1111\/bjh.17664"},{"key":"S0950268822001480_ref15","doi-asserted-by":"crossref","first-page":"215","DOI":"10.2741\/s459","article-title":"Interaction of the renin angiotensin and Cox systems in the kidney","volume":"8","author":"Quadri","year":"2016","journal-title":"Frontiers in Bioscience (Scholar Edition)"},{"key":"S0950268822001480_ref81","doi-asserted-by":"publisher","DOI":"10.1084\/jem.20181359"},{"key":"S0950268822001480_ref58","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbi.2020.05.037"},{"key":"S0950268822001480_ref109","doi-asserted-by":"publisher","DOI":"10.1097\/MBC.0000000000000512"},{"key":"S0950268822001480_ref98","doi-asserted-by":"publisher","DOI":"10.1111\/jth.12977"},{"key":"S0950268822001480_ref35","first-page":"799","article-title":"At the heart of COVID-19 [published online ahead of print May 5, 2020]","volume":"72","author":"Khan","year":"2020","journal-title":"Journal of Cardiac Surgery"},{"key":"S0950268822001480_ref115","doi-asserted-by":"publisher","DOI":"10.1007\/s11239-021-02457-9"},{"key":"S0950268822001480_ref5","doi-asserted-by":"publisher","DOI":"10.1002\/jmv.26720"},{"key":"S0950268822001480_ref79","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2019.03.005"},{"key":"S0950268822001480_ref112","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2141.2008.07074.x"},{"key":"S0950268822001480_ref50","doi-asserted-by":"publisher","DOI":"10.1016\/j.jacbts.2020.09.003"},{"key":"S0950268822001480_ref97","doi-asserted-by":"publisher","DOI":"10.1186\/s40560-014-0065-0"},{"key":"S0950268822001480_ref24","doi-asserted-by":"publisher","DOI":"10.1016\/S0140-6736(20)30566-3"},{"key":"S0950268822001480_ref103","doi-asserted-by":"publisher","DOI":"10.1016\/S2352-3026(20)30216-7"},{"key":"S0950268822001480_ref117","doi-asserted-by":"publisher","DOI":"10.1016\/j.thromres.2020.06.027"},{"key":"S0950268822001480_ref56","doi-asserted-by":"publisher","DOI":"10.1021\/acschemneuro.0c00122"},{"key":"S0950268822001480_ref107","doi-asserted-by":"publisher","DOI":"10.1111\/jth.14374"},{"key":"S0950268822001480_ref47","doi-asserted-by":"publisher","DOI":"10.1016\/j.lfs.2020.117723"},{"key":"S0950268822001480_ref3","doi-asserted-by":"publisher","DOI":"10.3390\/jcm9082624"},{"key":"S0950268822001480_ref28","first-page":"2022","article-title":"Renovascular complications in Covid19: a systematic review","volume":"14","author":"Kaur","year":"2022","journal-title":"International Journal of Early Childhood"},{"key":"S0950268822001480_ref54","doi-asserted-by":"publisher","DOI":"10.3389\/fpsyt.2020.00860"},{"key":"S0950268822001480_ref10","doi-asserted-by":"publisher","DOI":"10.1016\/j.micpath.2020.104621"},{"key":"S0950268822001480_ref32","doi-asserted-by":"publisher","DOI":"10.3889\/oamjms.2022.9431"},{"key":"S0950268822001480_ref1","doi-asserted-by":"publisher","DOI":"10.3390\/jcm9113630"},{"key":"S0950268822001480_ref48","doi-asserted-by":"publisher","DOI":"10.1186\/s12931-020-01352-w"},{"key":"S0950268822001480_ref37","doi-asserted-by":"publisher","DOI":"10.1016\/S2213-2600(20)30076-X"},{"key":"S0950268822001480_ref26","first-page":"1","article-title":"COVID-19 and the kidney: time to take a closer look","volume":"54","author":"Liakopoulos","year":"2021","journal-title":"International Urology and Nephrology"},{"key":"S0950268822001480_ref6","doi-asserted-by":"publisher","DOI":"10.1016\/j.euf.2020.06.002"},{"key":"S0950268822001480_ref78","first-page":"989","article-title":"Pernio (chilblains), SARS-CoV-2, and COVID toes unified through cutaneous and systemic mechanisms. in mayo clinic proceedings","volume":"96","author":"Cappel","year":"2021","journal-title":"Elsevier"},{"key":"S0950268822001480_ref11","doi-asserted-by":"publisher","DOI":"10.1002\/rmv.2176"},{"key":"S0950268822001480_ref93","doi-asserted-by":"publisher","DOI":"10.1016\/S2352-3026(20)30145-9"},{"key":"S0950268822001480_ref88","doi-asserted-by":"publisher","DOI":"10.1186\/s12950-020-00263-3"},{"key":"S0950268822001480_ref67","doi-asserted-by":"publisher","DOI":"10.1016\/j.expneurol.2021.113837"},{"key":"S0950268822001480_ref33","doi-asserted-by":"publisher","DOI":"10.1016\/j.ipej.2020.08.001"},{"key":"S0950268822001480_ref44","doi-asserted-by":"publisher","DOI":"10.1016\/j.ijcha.2020.100589"},{"key":"S0950268822001480_ref60","doi-asserted-by":"publisher","DOI":"10.1007\/s44229-022-00010-1"},{"key":"S0950268822001480_ref23","doi-asserted-by":"publisher","DOI":"10.1136\/bmj.m1091"},{"key":"S0950268822001480_ref69","doi-asserted-by":"publisher","DOI":"10.3389\/fmed.2021.745789"},{"key":"S0950268822001480_ref100","doi-asserted-by":"publisher","DOI":"10.1084\/jem.20201129"}],"container-title":["Epidemiology and Infection"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.cambridge.org\/core\/services\/aop-cambridge-core\/content\/view\/S0950268822001480","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,23]],"date-time":"2023-05-23T09:38:24Z","timestamp":1684834704000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.cambridge.org\/core\/product\/identifier\/S0950268822001480\/type\/journal_article"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022]]},"references-count":119,"alternative-id":["S0950268822001480"],"URL":"https:\/\/doi.org\/10.1017\/s0950268822001480","relation":{},"ISSN":["0950-2688","1469-4409"],"issn-type":[{"value":"0950-2688","type":"print"},{"value":"1469-4409","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022]]},"assertion":[{"value":"Copyright \u00a9 The Author(s), 2022. Published by Cambridge University Press","name":"copyright","label":"Copyright","group":{"name":"copyright_and_licensing","label":"Copyright and Licensing"}},{"value":"This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http:\/\/creativecommons.org\/licenses\/by\/4.0\/), which permits unrestricted re-use, distribution and reproduction, provided the original article is properly cited.","name":"license","label":"License","group":{"name":"copyright_and_licensing","label":"Copyright and Licensing"}},{"value":"This content has been made available to all.","name":"free","label":"Free to read"}],"article-number":"e208"}}